Ocean Outbreak: Confronting the Rising Tide of Marine Disease

By Drew Harvell

Winner of the Sustainability Science Award 2020, Ecological Society of America
Winner of the PROSE Award (Biological Sciences category) 2020, Association of American Publishers

There is a growing crisis in our oceans: mysterious outbreaks of infectious disease are on the rise. Marine epidemics can cause mass die-offs of wildlife from the bottom to the top of food chains, impacting the health of ocean ecosystems as well as lives on land. Portending global environmental disaster, ocean outbreaks are fueled by warming seas, sewage dumping, unregulated aquaculture, and drifting plastic.

Ocean Outbreak follows renowned scientist Drew Harvell and her colleagues into the field as they investigate how four iconic marine animals—corals, abalone, salmon, and starfish—have been devastated by disease. Based on over twenty years of research, this firsthand account of the sometimes gradual, sometimes exploding impact of disease on our ocean’s biodiversity ends with solutions and a call to action. Only through policy changes and the implementation of innovative solutions from nature can we reduce major outbreaks, save some ocean ecosystems, and protect our fragile environment.

 

• Language: English
• Publisher: University of California Press
• Release date: Apr 16, 2019
• ISBN: 9780520969506

Drew Harvell

Drew Harvell is Professor of Ecology at Cornell University, Curator of the Blaschka Glass Marine Invertebrate Collection, and author of Ocean Outbreak: Confronting the Rising Tide of Marine Disease.

Book preview

Ocean Outbreak

The publisher and the University of California Press Foundation gratefully acknowledge the generous support of the Ralph and Shirley Shapiro Endowment Fund in Environmental Studies.

Ocean Outbreak

Confronting the Rising Tide of Marine Disease

DREW HARVELL

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UNIVERSITY OF CALIFORNIA PRESS

University of California Press, one of the most distinguished university presses in the United States, enriches lives around the world by advancing scholarship in the humanities, social sciences, and natural sciences. Its activities are supported by the UC Press Foundation and by philanthropic contributions from individuals and institutions. For more information, visit www.ucpress.edu.

University of California Press

Oakland, California

© 2019 by C. Drew Harvell

Library of Congress Cataloging-in-Publication Data

Names: Harvell, C. Drew, 1954– author.

Title: Ocean outbreak : confronting the rising tide of marine disease / Drew Harvell.

Description: Oakland, California : University of California Press, [2019] | Includes bibliographical references and index. |

Identifiers: LCCN 2018049384 (print) | LCCN 2018051515 (ebook) | ISBN 9780520969506 | ISBN 9780520296978 (cloth : alk. paper)

Subjects: LCSH: Marine ecosystem health. | Corals—Diseases. | Abalones—Diseases. | Salmon—Diseases. | Starfishes—Diseases.

Classification: LCC QH541.5.S3 (ebook) | LCC QH541.5.S3 H37 2019 (print) | DDC 577.7—dc23

LC record available at https://lccn.loc.gov/2018049384

Manufactured in the United States of America

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To cherish what remains of the Earth and to foster its renewal is our only legitimate hope of survival.

Wendell Berry

Contents

List of Illustrations

Preface

1. What Rises with the Tide?

2. Coral Outbreaks

A Global Threat to Marine Biodiversity

3. Abalone Outbreaks

A Steady Path to Extinction?

4. Salmon Outbreaks

Food from the Ocean Imperiled

5. Starfish Outbreaks

An Ecological Domino Effect

6. Nature’s Services to the Rescue

Afterword: The Next Big Outbreak

References

Index

Illustrations

MAPS

1. World coral reef distribution

2. Southeast Asia and Indonesia

3. Central California abalone survey sites

4. Fraser River, Discovery Islands, and Salish Sea

5. Atlantic salmon farms in British Columbia

6. Starfish epidemic locations

FIGURES

1. Mass mortality of the sunflower star, British Columbia, 2013

2. Lesions in a sea fan caused by Aspergillus sydowii

3. The epidemiologic triad

4. Yellow band lesion growth in relation to temperature

5. Abalone on Santa Cruz Island, 1986 and 1988

6. Abalone species from California

7. Surveys of black abalone, central California coast, 1992–2001

8. Comparison of a sick abalone with a healthy abalone

9. Susceptibility of three species of abalone to withering foot syndrome

10. Mortality of the ochre star in Bamfield, British Columbia

11. Urchin barrens in Sechelt Inlet, British Columbia

12. Decline of the sunflower star during a marine heat wave

13. Enterococcus colonies on test plates from Barrang Lompo

14. Average counts of Enterococcus colonies on test plates from the Spermonde Archipelago

15. How filter feeders alter pathogen transmission

Preface

In the aftermath of a devastating outbreak that brought ocean disease to the public eye in 2015, I was invited to organize an Ocean Outbreaks Day during which members of Congress would be briefed on growing threats to organisms in our coastal waters. Our team of four scientists traveled to Washington, DC, and gave talks on diseases that were plaguing reefs in Florida and Hawaii, impacting oyster fisheries in North Carolina and elsewhere along the eastern seaboard, threatening lobster fisheries in Long Island and Maine, and causing harm to salmon fisheries in Washington and abalone in California. Throughout our presentations we emphasized how disease outbreaks in US coastal waters had economic consequences.

There was keen bipartisan interest in ocean health that day. However, the questions we received from lawmakers and their staffers revealed to us a large information gap. Those from ocean states were knowledgeable about some issues affecting the sustainability of our oceans. They were aware of overfishing and the need for a restructuring of fisheries management. They knew about nutrient pollution and eutrophication and the dangers of polluting the oceans with both large plastics and insidious micro-plastics. They had concerns about the emerging problem of ocean acidification and its effects on organisms that make calcareous shells. Even if the impacts still seemed far off, staffers and legislators from Hawaii and Florida were aware that warming temperatures were bringing devastation to coral reefs around the world. But few people in the hearing rooms were more than vaguely aware of the rolling tide of new disease outbreaks that is affecting marine organisms around the world. They did not know that warmer and more polluted ocean waters are allowing many infectious pathogens to thrive while at the same time weakening marine creatures’ abilities to withstand disease.

•    •    •

Most policymakers we briefed had never thought about what would happen to their state’s economies if warming oceans made for sicker marine organisms. They were clearly concerned, and it was motivating to see them respond constructively. Their excitement was palpable as staffers brainstormed about new legislation focused on ocean health. Many of them indicated their support for a new bill introduced by Congressman Dennis Heck of Washington, the Emergency Marine Disease Act (which ultimately failed to pass).

In that moment, I realized the urgent need for scientists to communicate to citizens and policymakers what we are learning about marine disease. We need to tell the stories of what we discover in the lab and the field. We need to translate our data and findings into forms that make the public more aware of the seriousness of the threats that ocean pathogens pose to our food supplies, economies, livelihoods, and health. We need to propose ways to protect the health of the oceans and better manage our impacts. That was the moment I resolved to do my part in this effort. After much reflection, I decided that a book detailing my experiences with four recent and serious disease outbreaks might be the best way to raise public awareness of the threat of marine diseases and motivate others to take action.

It takes a village to write a book like this and I am grateful to my friends, colleagues, and family members for their help and encouragement. My son Nathan, himself a writer, helped with hours of editing and ideas in the formulation, proposal writing, and early versions of the book. My daughter Morgan commented on the corals chapter. My husband Chuck listened patiently, advised on oceanographic issues, and helped brainstorm titles and frame ideas.

Substantive early help came from Steve Palumbi and Peter Sale, who read and advised on an early version. Developmental editor Eric Engles read every word twice and was a constant force in helping me translate my ideas from the ivory tower to a place closer to real lives.

The people in my research lab at Cornell have been mainstays of help, guidance, and fact-checking. Phoebe Dawkins edited, suggested good ideas and new wording, fact-checked, prepared literature lists, corrected spelling, prepared figures, and advised on maps, all with genuine enthusiasm and unceasing encouragement. Putu Dawkins drew the maps. Allison Tracy read, revised, and made suggestions on several chapters, including those about corals and salmon and the final chapter. Morgan Eisenlord helped with the starfish chapter and Olivia Graham with the final chapter. Joleah Lamb provided help on both the corals chapter and the final chapter. Cornell undergraduates in my research apprenticeship semester also commented on some sections.

My colleagues were generous with their time, helping me with fact-checking and related matters. Colleen Burge reviewed the chapters on abalone and starfish. Ian Hewson reviewed the starfish chapter; Carolyn Friedman and Brian Tissot the chapter on abalone; and Maya Groner, Paul Hershberger, and Kim Sundberg the chapter about salmon. At the eleventh hour, Scott Schwinge and Joe Gaydos read the entire book and helped weed out many extra references.

I am grateful to the team at the University of California Press: Kate Marshall, for supporting the concept and the book from the beginning; Dore Brown, for shepherding the book through the production process; and Jan Spauschus, for thoughtful copy editing.

I appreciate National Science Foundation funding of our Ocean Health Research Coordination Network. Ocean Outbreak communicates themes developed over the five years of that project and the views of the many scientists involved. Funding from the Atkinson Center at Cornell, the Nature Conservancy, and the Environmental Defense Fund facilitated the work in Indonesia and Myanmar.

CHAPTER ONE

What Rises with the Tide?

It is the microbes that will have the last word.

Louis Pasteur

You always remember the moment something bad turns big. For me, a bad situation assumed epic proportions in December 2013 when I was at the Nature Conservancy’s All Science Meeting in California. I received an email from my colleague Pete Raimondi saying that thousands of starfish from at least ten species were dying fast in the waters around Monterey, California. I already knew that a species of giant sunflower starfish (Pycnopodia helianthoides) was dying catastrophically hundreds of miles to the north, not far from my home on San Juan Island in northwest Washington State. I had seen underwater photographs taken by Neil McDaniel near Vancouver, Canada, showing a disaster unfolding in the deep canyons there. In photos taken on October 19, the rock cliffs were covered with healthy-looking stars. In photos taken only ten days later, all that was left were hundreds of dead bodies piled on the sea floor beneath the cliffs (see figure 1). We had assumed this was a localized event affecting a single species, like others we had seen. Doubts about the geographic restriction of the starfish die-off had surfaced, however, when we learned in November, only a few weeks before the Nature Conservancy’s meeting, that the Vancouver, Seattle, and Monterey aquariums had each lost hundreds of stars in their tanks. Against this background, Pete’s email signaled something much more worrisome than a local die-off of one kind of starfish. It seemed we were seeing the beginnings of a disease outbreak that could end up affecting starfish along the entire Pacific coast.

Figure 1. Mass mortality of the sunflower star over two weeks in British Columbia, 2013. Photos by Neil McDaniel.

In addition to being concerned about the broad geographic extent of the outbreak, I was worried that it involved starfish, and not just one species but many. Starfish may seem innocuous and almost inanimate given the glacial pace at which most species move, but they are the lions of our seascape. Even a few starfish can control the structure and composition of the surrounding ecosystem by eating huge numbers of the mussels and oysters that would otherwise dominate. Observing ochre stars preying on mussels and the changes that occurred when he removed them, experimentally, from his study areas on Tatoosh Island caused Bob Paine, one of my mentors, to invent the term keystone species. Added to that, the West Coast of the United States has a bright medley of different starfish species, second only to Australia for temperate waters. There are approximately eighty species described in the eminent marine biologist Eugene Kozloff’s key for Puget Sound and the San Juan Islands in Washington. The catastrophic loss of not only ochre stars but other species as well over a broad swath of ocean could have a domino effect on ocean ecology, causing a cascade of changes that might ultimately impact animals—such as abalone and salmon—that humans depend on for food.

I left my session early and called Pete to hear firsthand what he and his fellow divers had seen in Monterey. He told me that they had watched the giant sunflower stars die first: they lost strength in their tube feet, their arms tore off and crawled away from their bodies, and their organs spilled out, leaving the stars to fall off the rock walls and docks. A week later, they had watched the same thing happen to other species. Sun stars (Solaster sp.), rainbow stars (Orthasterias koehleri), giant pink stars (Pisaster brevispinus), giant stars (Pisaster giganteus), mottled stars (Evasterias troschelii), vermillion stars (Mediaster aequalis), and bat stars (Patiria miniata) all began to die rapidly in high numbers. One of the last to go was the ochre star (Pisaster ochraceus). The sea bottom, Pete told me, was littered with dead, decaying starfish arms and bodies, with crabs picking at them. The only species left gripping the rocks were the leather star (Dermasterias imbricata) and the blood star (Henricia spp).

It took me a moment to get past the gruesomeness of Pete’s descriptions and assess their import. Many different species were dying over a very wide geographic range, from Vancouver all the way to Monterey on California’s central coast. Almost all the most common starfish species were affected. Captive aquarium populations were being hit as badly as wild ones. They were dying rapidly, and few if any were surviving. It seemed unlikely that the culprit was some kind of horrific new coast-wide pollution problem—the die-off was too widespread. I had to conclude that we were facing a new marine epidemic, a disease that was killing an astonishing number of different species at a blistering pace and with a vast geographical reach.

The Nature Conservancy meeting turned hectic for me after I talked with Pete. I tried to attend sessions but my phone was ringing almost non-stop. One call was from Katie Campbell, a broadcast reporter with KCTV in Seattle. She wanted help with a television news story about all the dead starfish washing up on the beaches around the city. She had been told to call me because I lead a government-funded research network that specializes in ocean disease outbreaks and I teach an ecology of infectious disease course at the University of Washington marine lab near Seattle. I filled her in on what I knew about the event. When we finished our conversation, I thought, What am I doing at this meeting in California when stars are dying in large numbers in my home waters? The die-off was unfolding in full public view all over our beaches and people were upset and concerned. I checked my tide table and saw that if I made it to Seattle the next day I could catch a low tide at around 8:00 pm. If I went to the right place, I could immediately see how the outbreak looked and begin collecting data.

Soon I was back on the phone, talking with Laura James, who called to tell me stars were dying at her favorite dive site, Cove 1 at Alki Beach, right near downtown Seattle. Cove 1 is surprisingly diverse, housing giant pacific octopus and their babies, five species of sea star, urchins, crabs, sea slugs, and anemones. Laura, an obsessive and brilliant underwater videographer, told me that she first noticed stars falling off the pilings in late October. She had been worried and went back repeatedly to film the underwater horror that was unfolding.

Laura does a lot of diving in the dark at night. A few weeks earlier she had recorded nighttime video footage that she directed me to watch on my laptop. I stared at the screen as hundreds of ochre, mottled, and sunflower stars peeled off the pilings, arm by arm as tube feet lost their grip, the scene ghoulishly lit by Laura’s video lights. Some stars were so far gone that their bodies ripped away, leaving only an arm or two hanging, organs spilling out. Underneath, the pilings were surrounded by hundreds of decomposing stars slowly turning into a white bacterial mat. I told Laura I would come help and headed for the airport. It wasn’t the first time that I had dropped everything to jump on a plane to document a disease emergency. The scale and pace of starfish mortality seemed ominous and important to see firsthand. Like a crime scene, the site of a massive wildlife die-off contains hundreds of critical details to notice and record. To begin the process of understanding this event, to fit together the puzzle pieces, I needed to see the scene for myself. How many stars were on a beach? How many stars were dead? What sizes were they? How many were dying? Were the sick ones grouped together? Were the sick stars grouped on a warm area of the beach or near pollution or freshwater stresses? Was the beach a rocky ledge? Was it composed of rocky cobble, gravel, or sand? Indeed, it would soon be apparent that we were experiencing the largest epidemic in marine wildlife history, one that demonstrated how frighteningly fast an outbreak can spread and virtually eliminate an entire chunk of ocean biodiversity.

•    •    •

Our oceans and the life forms they support are under siege, threatened by a formidable collection of forces that cause both sudden mass mortalities and a slow degradation of biodiversity. The top threats are the warming and acidification that accompany climate change, over-fishing, pollution from human activities on land, nearshore dredging, and oil extraction. Faced with such a ponderous list, it is hard to prioritize. As a marine ecologist specializing in disease, I worry most about the threat posed by microbes, because in oceans beset by all these stresses, microscopic disease-causing organisms can gain the upper hand, cause death on a massive scale, and thereby bring about rapid, wide-scale ecological change.

Microbes are scary in part because they are changeable and not under our control. Pathogenic organisms in the microbe category—viruses, bacteria, fungi, protozoans, and other disease-causing agents that don’t fit neatly into these groups—are constantly evolving, their genetic codes often changing rapidly and staying one step ahead of their hosts’ defenses. Think about one of the deadliest of human diseases, the Ebola virus, which causes fever, severe headache, vomiting, diarrhea, and hemorrhagic bleeding in its victims. Available evidence indicates that the virus has existed in bats in Africa for a long time, occasionally jumping to human beings but never breaking out beyond Africa. Then in 2013 a horrific epidemic of Ebola virus started in Guinea, Liberia, and Sierra Leone, spreading faster and further in Africa than previous outbreaks. Declared a Health Emergency of Special Concern in August 2014, it ultimately killed over 11,000 people and reached Europe and North America. Why was this outbreak so much bigger than earlier ones? Scientists aren’t sure, but one hypothesis, backed up by intensive study of the changing viral genome during the epidemic done by a team led by Daniel Park of Harvard’s Broad Institute, is that a key mutation allowed it to become more transmissible among humans. Because viruses have a very short life span and so many new virus particles are produced in the body of a single host, there is ample opportunity for such mutations to occur.

Microbes are dangerous too, because many can

Reviews for Ocean Outbreak

[breic-1 · Rating: 4 out of 5 stars]

A fascinating story of Harvell's research into disease outbreaks in coral, abalone, salmon, and starfish, especially along the US West Coast. Harvell does a good explaining the science, as well as the process of the science, and balances this with her personal perspective. For me, the balance was perfect. This is a niche subject, but the book is accessible and not overly long.

I was disappointed, though, by how hard Harvell plugs more funding for her work as a "solution" to ocean outbreaks. Better monitoring of diseases will do nothing to ameliorate them. We cannot treat or vaccinate wild ocean species. Since these outbreaks are all connected to global warming, the only way to stop them is with policy changes to stop greenhouse gas pollution. Throwing Harvell and her collaborators a few million dollars seems worthwhile in terms of getting interesting science, but it won't solve any problems. (Possibly it could help with aquaculture outbreaks, or with localized pollution problems that cause disease.)

> The world's coral reefs, our most diverse and valuable marine ecosystems, are being sickened by a variety of factors all at once. Our only chance to limit their loss lies in understanding how all the threats to coral interact with and affect each other.

> With the threat of the imminent extinction of tropical corals, white abalone, and our sunflower star, and their cascading ecological impacts, we crossed a line in the sand. As a society, we can no longer stand by idly. We have let loose many destructive forces over which we have little control, but science can still make a difference. The problem is that inadequate funding remains a major impediment to scientists identifying the causes of disease outbreaks in the ocean, investigating the contributing factors, and developing solutions. … The whole thing would have played out differently if we had had the right resources from the start—not only funds from school children who stepped up to help, but also government funding. If the starfish outbreak was instead a deadly virus epidemic among humans, like Ebola, we would have had massive resources at our disposal to investigate the pressing questions surrounding the outbreak. Instead, many people acted as if this huge epidemic affecting a keystone species in the ocean was simply a curiosity and assumed scientists would figure it out.

A few other quotes:

> rickettsia is a very slowly incubating disease agent. It took almost a year before the abalone were conclusively infected. The long incubation period was also why the range of the pathogen initially looked much larger than the range of sick abalone … On land, rickettsial bacteria are never free living and can survive only inside the cells of a host. Scientist call them obligate intracellular parasites. They are always transmitted by a bite from an insect vector like a tick or a mite. Two diseases of terrestrial animals caused by rickettsial bacterial are Rocky Mountain spotted fever and typhus. It is tricky to confirm a rickettsia as the cause of a disease, since they hide inside cells and thus cannot be detected by a simple blood test. … since seawater has essentially the same salinity as abalone blood, the bacterium can survive briefly outside a host and can thus be transmitted in seawater. She and her student Lisa Crosson tested infectivity and found that the rickettsia remains viable in seawater for at least twenty-four hours. It is extraordinary that this rickettsial bacterium deviates from the normal transmission biology of requiring a vector on land

> A mere eight months after this Atlantic salmon spill, Governor Jay Inslee banned all Atlantic salmon farming in Washington State. His legislation will prevent new farms and will phase out all existing farming by 2025, bringing to an end three decades of non-native fish farming. Washington State now joins Alaska in banning commercial finfish aquaculture

> Following Bob's experimental manipulation, the stretch of shore without ochre stars became encrusted with what Bob called a "mussel glacier"—a huge dark mass of thousands of mussels packed together stretching from the subtidal to far up in the intertidal. The mussel bed crowded out many other species, like green sea anemones, green sponges. and pinkish sea squirts … Bob coined the term keystone species in a 1969 note about food webs for the kind of ecological role the starfish assumed in the rocky intertidal.

> a big outbreak of disease in sunflower stars in British Columbia. On the blog of echinoderm expert Chris Mah, Echinoblog, people were posting striking photos

> The almost complete loss of the mighty sunflower stars and several other species in deeper waters has allowed a huge influx of sea urchins, whose populations from California to Alaska had previously been controlled by the voracious sunflowers. The hordes of hungry sea urchins have decimated kelp beds … A paper published in 2018 by a team of scientists from the University of California at Merced, led by Laura Schiebelhut, reported some very good news: big increases in populations of the ochre stars and newly recruited baby stars that were growing up. Most exciting, their complete genetic analysis of stars before the outbreak compared to after the outbreak showed a big genetic change. They suggested that the epidemic had killed all the susceptible stars and the survivors were hardy genetic stock that was resistant to the virus. The bad news is that new surveys in 2017 show that the sunflower star is virtually gone from California to Alaska.

> I find it particularly galling that the entire municipality of Victoria, Canada dumps all its sewage, untreated, into the richest waters on our continent